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Alfred Maroyi /J. Pharm. Sci. & Res. Vol. 11(10), 2019, 3420-3428

A review of medicinal uses, phytochemistry and biological activities of angustifolia

Alfred Maroyi Department of Biodiversity, University of Limpopo, Private Bag X1106, Sovenga 0727, South .

Abstract Boscia angustifolia is an evergreen shrub or small tree widely used as herbal medicine in the and sub-Saharan Africa. The current study critically reviewed the botany, medicinal uses, phytochemistry and biological activities of B. angustifolia. Literature on botany, medicinal uses, phytochemical and biological activities of B. angustifolia was collected from multiple internet sources including Elsevier, Google Scholar, SciFinder, Web of Science, Pubmed, BMC, Science Direct and Scopus. Complementary information was gathered from pre-electronic sources such as books, book chapters, theses, scientific reports and journal articles obtained from the University library. This study revealed that the species is used as cholagogue and purgative, and herbal medicine for bruises, sores and wounds, gastro-intestinal problems, eye problems and otitis, fever and typhoid fever, gonorrhoea and venereal diseases, malaria, respiratory infections, skin problems, swellings and swollen feet, ulcers and ethnoveterinary medicine. Ethnopharmacological research identified alkaloids, amino acid derivatives, carboxylic acids and their derivatives, saponins, sugars and their derivatives from the bark, fruits, leaves and roots of B. angustifolia. The crude extracts of the species and the compound 7,4'-dimethoxy quercetin isolated from the species exhibited antibacterial, antimycobacterial, antifungal, antiviral, antioxidant, antiplasmodial, antitrypanosomal, GABAA– benzodiazepine receptor binding, larvicidal and cytotoxicity activities. Boscia angustifolia should be subjected to detailed phytochemical, pharmacological and toxicological evaluations aimed at correlating its medicinal uses with its phytochemistry and pharmacological activities. Keywords: Boscia angustifolia, , herbal medicine, indigenous knowledge, Sahel, sub-Saharan Africa

INTRODUCTION and sub-Saharan Africa, and therefore, there is need for Boscia angustifolia A. Rich. is an evergreen shrub or small formal documentation and systematic research which is tree belonging to the Capparaceae or Capparidaceae or beneficial to indigenous and traditional systems of herbal caper family. The Capparaceae family contains 33 genera medicine.30,31 It is within this context that this review was and approximately 700 species distributed in tropical and undertaken aimed at reviewing the botany, medicinal uses subtropical regions of the world.1-3 Boscia Lam. is a genus and biological activities of B. angustifolia so as to provide of shrubs or small trees consisting of 37 species, mostly in baseline data required in evaluating the therapeutic tropical and southern Africa, a few in Madagascar, one potential of the species. confined to Arabia, mostly in semi-arid or seasonally dry areas.2,4,5 Several Boscia species are used as herbal Botanical profile of Boscia angustifolia medicines in tropical Africa and these include B. The genus name Boscia is in honour of a French naturalist, albitrunca (Burch.) Gilg & Gilg-Ben., B. angustifolia, B. botanist, zoologist and horticulturist Louis Auguste coriacea Graells, B. foetida Schinz, B. longifolia Hadj- Guillaume Bosc (1759-1828).32 The species name Moust., B. madagascariensis (DC.) Hadj-Moust., B. “angustifolia” means “narrow-leaved” in reference to mossambicensis Klotzsch., B. salicifolia Oliv. and B. narrow oblong and sometimes wider leaves.4,33 Two senegalensis Lam.6-8 Iwu6 argued that the medicinal infraspecies of B. angustifolia are recognized, namely B. properties of Boscia species could be attributed to angustifolia var. angustifolia with glabrous leaves alkaloids, flavonoids, sesquiterpenes and their glycosides, occurring from to , and northern sulphur compounds and lipids that are associated with the Tanzania and var. corymbosa (Gilg) DeWolf with short genus. Boscia angustifolia is categorized as a and hairy leaves below and occurring from Uganda and multipurpose species in , Ethiopia, Eritrea Kenya southward to northern South Africa.7,34-40 However, and Tanzania, used as a source of charcoal, cosmetics, dye most ethnobotanical and ethnopharmacological literature or tannin, fodder, food, firewood, construction materials, do not separate B. angustifolia into specific varieties, but ethnoveterinary medicines, herbal medicines, shade, rather to B. angustifolia sensu lato, and this is the fodder, source of bee forage, toothbrush, reclaiming approach that has been adopted in this study. degraded sites and source of timber for furniture and carvings.9-27 The fruits of B. angustifolia are edible but Boscia angustifolia is commonly referred to as “rough- bitter, however, seeds are cooked and then eaten.28 The leaved shepherd tree” in English. Synonyms associated powdered seeds are mixed with millet (Eleusine coracana with B. angustifolia include B. caloneura Gilg, B. Gaertn.) flour and added to soups or cereals.28 Boiled corymbosa Gilg, B. dawei Sprague & M.L. Green, B. pieces of wood have been used to sweeten milk7 and the engleri Gilg & Gilg-Ben., B. fischeri Pax, B. homblei De bark of B. angustifolia has been used as tea in Kenya.29 Wild., B. patens Sprague & M.L. Green, B. reticulata Boscia angustifolia appears to be an important source of Hochst. ex A. Rich. and Boscia senegalensis Hochst. ex herbal medicine within its distributional range in the Sahel Walp.34-37,39,40 Boscia angustifolia is an evergreen shrub or

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small tree with rigid and sometimes spiny branches in drier regions with rainfall ranging from 200 mm to 800 growing up to 15 m in height.7,38,41 The bole is often mm per annum.7,24 deeply and sinuously fluted and twisted with pale grey bark. The leaves are often spirally arranged or occur in Medicinal uses of Boscia angustifolia groups of two to four on very dwarf spur-branchlets.38 The The bark, bark fibres, fruits, leaves, roots, stem bark and leaves are elliptic to oblanceolate in shape, leathery, dark twigs of B. angustifolia are mainly used as cholagogue and green in colour above, much paler and grey-green or purgative, and herbal medicine for bruises, sores and bluish green below. The flowers are small, sweet-smelling wounds, gastro-intestinal problems, eye problems and and yellowish green in colour, occurring in dense clusters otitis, fever and typhoid fever, gonorrhoea and venereal on short terminal lateral shoots. The fruit is a berry, which diseases, malaria, respiratory infections, skin problems, is spherical in shape, hairless and yellowish to almost swellings and swollen feet, ulcers and ethnoveterinary black in colour with one to two seeds embedded in a sticky medicine (Table 1, Figure 1). In Zimbabwe, the roots of B. pulp.36,38 Boscia angustifolia is widespread, from southern angustifolia are mixed with roots of Vernonia glabra Arabia and , Senegal and Gambia eastward to (Steetz) Vatke as herbal medicine for constipation.47 In Somalia and southward to northern South Ethiopia, the twigs and roots of B. angustifolia are mixed Africa.34,35,37,40,43-46 The species has been recorded in dry, with those of Capparis tomentosa Lam., Carissa spinarum open woodland, bushveld, wooded grassland, often on L., Croton macrostachyus Hochst. ex Delile, Phytolacca termitaria, also on hills, stony or rocky soils, laterite dodecandra L'Hér., Ruta chalepensis L., Securidaca outcrops and cliffs, loamy soils, and sometimes dry longipedunculata Fresen. and Sida schimperiana Hochst. riverbeds at an altitude up to 2000 m above sea level and ex A. Rich. and used against evil spirits and evil eye.48-54

Table 1: Medicinal applications of Boscia angustifolia Medicinal use Parts of the used Country References Anthelmintic Bark, leaves, roots and stem bark Elegami et al.55 Kenya, , Keay et al.56; Diallo et al.57; Bruises, sores and Bark, leaves and roots and Fowler58; Hassan et al.59; wounds Zambia Cheruiyot et al.60; Chalo et al.61 Cholagogue Leaves Mali and Senegal Chini et al.62; Diallo et al.63 Roots mixed with roots of Constipation Zimbabwe Gelfand et al.47 Vernonia glabra (Steetz) Vatke Gidey et al.27; Keay et al.56; Gastro-intestinal Ethiopia, Kenya, Hassan et al.59; Chalo et al.61; problems (diarrhoea, Bark, leaves, roots and stem bark Mali, Nigeria and Ahua et al.64; Maregesi et al.65; dysentery and intestinal Tanzania Omwenga et al.66; Mariita et disorder) al.67; Omwenga et al.68 Dislocated backbone Roots Ethiopia Gidey et al.27 Twigs and roots mixed with Capparis tomentosa Lam., Carissa Zenebe et al.48; Enyew et al.49; spinarum L., Croton Chekole et al.50; Gidey and Magical purposes (evil macrostachyus Hochst. ex Delile, Ethiopia Asfaw51; Hishe and Asfaw52; spirits and evil eye) Phytolacca dodecandra L'Hér., Mekuanent et al.53; Fitsumbirhan Ruta chalepensis L., Securidaca et al.54 longipedunculata Fresen. and Sida schimperiana Hochst. ex A. Rich. Chini et al.62; Gebrezgabiher et Eye problems and otitis Bark and leaves Ethiopia and Mali al.69 Fertility Roots Zambia Fowler58 Burkina Faso, Keay et al.56; Hassan et al.59; Fever and typhoid fever Bark, leaves, roots and twigs Kenya and Cheruiyot et al.60; Fowler70 Nigeria Gonorrhoea and Kenya and Maregesi et al.65; Mariita et al.67; Bark and stem bark venereal diseases Tanzania Omwenga et al.68 Headache Bark Mali Diallo et al.63; Ahua et al.64 Human immunodeficiency virus Roots Zambia Chinsembu et al.71 (HIV) Hypertension Stem Nigeria Ajayi et al.72 Insanity Bark and roots Tanzania Mathias73 Joint pains Bark Kenya Chalo et al.61

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Medicinal use Parts of the plant used Country References Fowler70; Koch et al.74; Bizimana Bark, bark fibres, leaves, stem bark Kenya, Mali and Malaria et al.75; Kokwaro76; Chinsembu77; and twigs Zambia Diarra et al.78; Muthaura et al.79 Neuralgia Bark Mali Chini et al.62 Pain Leaves Mali Danton et al.80 Pesticide Leaves and stems Kenya Menge et al.81; Karani et al.82 Bark, fruits, leaves, roots and stem Purgative Mali and Sudan Elegami et al.55; Chini et al.62 bark Respiratory infections (chest pains, cough, Ethiopia, Kenya, Keay et al.56; Hassan et al.59; pneumonia, throat Bark, leaves and roots Nigeria and Cheruiyot et al.60; Mariita et al.67; infection and Tanzania Otieno et al.83; Legesse84 tuberculosis) Retained after birth Leaves and stems Kenya Kaingu et al.85 Snake bite Roots and stem bark Eritrea Kaushik et al.86 Skin problems (boils and Nigeria and Keay et al.56; Hassan et al.59; Leaves, roots and stem bark mumps) Tanzania Maregesi et al.65 Ethiopia, Kenya, Chalo et al.61; Diallo et al.63; Swellings and Swollen Bark Senegal and Doka and Yagi87; Tefera and feet Sudan Kim88 Ulcers (gastric and Namibia and Chinsembu et al.71; Chinsembu et Roots genital) Zambia al.89 Urinary infections Leaves and roots Nigeria Keay et al.56; Hassan et al.59 Kaingu et al.85; Tsigemelak et Vomiting Bark, leaves and stems Kenya al.90 Weight loss Leaves Burkina Faso Pare et al.91 Ethnoveterinary Bein et al.14; Zorloni23; Eritrea, Ethiopia, medicine (ectoparasites, Mekuanent et al.52; Bark, leaves and roots Kenya and fever, gynaecological Gebrezgabiher et al.69; Uganda problems and wounds) Byaruhanga et al.92; Kigen et al.93

Gastro-intestinal problems Respiratory infections Ethnoveterinary medicine Bruises, sores and wounds Swellings and swollen feet Malaria Fever and typhoid fever Skin problems Gonorrhoea and venereal diseases Ulcers Purgative Eye problems and otitis Cholagogue

0 1 2 3 4 5 6 7 8 9 10

Literature records No. of countries

Figure 1. Medicinal applications of Boscia angustifolia derived from literature records

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Phytochemical and nutritional composition of Boscia identified from the bark, fruits, leaves and roots of B. angustifolia angustifolia.7,19,20,59,62,66,67,94,95 Some of the Several compounds which include alkaloids, amino acid pharmacological activities associated with the species derivatives, carboxylic acids and their derivatives, could be attributed to the documented phytochemical saponins, sugars and their derivatives (Table 2) have been compounds.

Table 2: Phytochemical composition of Boscia angustifolia Phytochemical and nutritional composition Value Plant part Reference 1-Methyl imino thieno [3,4b] naphthalene (%) 10.0 Leaves Salem et al.94 1, 2, 4-Trimethoxy-5,6-dihydrophenanthridin-6-one (%) 2.4 Leaves Salem et al.94 1-H-9-methoxybenz [f] indole (%) 1.9 Leaves Salem et al.94 1,5-Anhydro-d-sorbitol (%) 1.1 Leaves Salem et al.94 2,3,4,5-Tetrahydroxypentanoic acid-1,4-lactone (%) 0.2 Leaves Salem et al.94 2-Deoxy-erythro-pentonic acid (%) 0.3 Leaves Salem et al.94 2-Hydroxy-4-methylpentanoic acid (%) 0.2 Leaves Salem et al.94 4-hydroxystachydrine - Bark and leaves Chini et al.62 4-N,N dimethylaminobutyric acid (%) 0.5 Leaves Salem et al.94 7,4'-dimethoxy quercetin - Leaves Salem et al.94 Acid detergent fibre (g/kg dry matter) 390.3 Leaves Osuga et al.20 Acid detergent lignin (g/kg dry matter) 94.9 Leaves Osuga et al.20 Allofuranose (%) 0.5 Leaves Salem et al.94 Ash (g/100g of dry matter) 8.0 Fruits Lemmens7 Ash (g/kg dry matter) 115.0 Leaves Dereje and Udén19 Calcium (g/kg dry matter) 22.0 Leaves Dereje and Udén19 Carbohydrates (g/100g of dry matter) 78.0 Fruits Lemmens7 Condensed tannins (g/kg dry matter) 22.7 Leaves Dereje and Udén19 149.4 – Dereje and Udén19; Crude protein (g/kg dry matter) Leaves 206.0 Osuga et al.20 Dry matter (g/kg dry matter) 405.0 Leaves Dereje and Udén19 Energy (kj/100g) 78.0 Fruits Lemmens7 Erythritol (%) 0.6 Leaves Salem et al.94 Esculetin - Leaves Salem et al.95 Esculetin 6,7 di-methylether - Leaves Salem et al.95 Fat (g/100g of dry matter) 5.0 Fruits Lemmens7 Fibre (g/100g of dry matter) 2.0 Fruits Lemmens7 Fructofuranose (%) 5.8 Leaves Salem et al.94 Glucopyranose (%) 0.3 Leaves Salem et al.94 Glucuronic acid lactone (%) 0.3 Leaves Salem et al.94 Glycerol (%) 2.5 Leaves Salem et al.94 Glycolic acid (%) 0.4 Leaves Salem et al.94 Gulonic acid lactone (%) 0.4 Leaves Salem et al.94 Hexadecanoic acid (%) 0.7 Leaves Salem et al.94 Hydracrylic acid (%) 0.5 Leaves Salem et al.94 in vitro dry matter digestibility (IVDMD) (g/kg dry matter) 0.5 Leaves Dereje and Udén19 Lactic acid (%) 18.1 Leaves Salem et al.94 Lactulose (%) 1.8 Leaves Salem et al.94 Malic acid (%) 1.0 Leaves Salem et al.94 Maltose methyloxime (%) 15.2 Leaves Salem et al.94 Mannitol (%) 1.6 Leaves Salem et al.94 Methyl-3-H pyrrolo [1,2a] indole-9-carboxylate (%) 0.5 Leaves Salem et al.94 Methyl-4-methoxy benzoate - Leaves Salem et al.95 Methyl galactoside (%) 0.3 Leaves Salem et al.94 Methyl leucine (%) 1.5 Leaves Salem et al.94 Methyl mannofuranoside (%) 0.2 Leaves Salem et al.94 Myo-inositol (%) 0.4 Leaves Salem et al.94 Neutral detergent fibre (g/kg dry matter) 570.4 Leaves Osuga et al.20 N, N-dimethyl methyl ester (%) 0.2 Leaves Salem et al.94 Organic matter (g/kg dry matter) 885.0 – Leaves Dereje and Udén19;

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Phytochemical and nutritional composition Value Plant part Reference 919.4 Osuga et al.20 Pentenal (%) 1.0 Leaves Salem et al.94 Phosphorus (g/kg dry matter) 2.4 Leaves Dereje and Udén19 Phthalic acid decyl octyl ester - Leaves Salem et al.95 Proteins (g/100g of dry matter) 7.0 Fruits Lemmens7 Quinic acid (%) 2.5 Leaves Salem et al.94 Rhamnocitrin-4'-O-methylether - Leaves Salem et al.95 Rhamnocitrin-3-O-β-glucopyranoside - Leaves Salem et al.95 Rhamnocitrin-3-O-β-(6"-O-E-p-coumaroyl)- - Leaves Salem et al.95 glucopyranoside Rhamnocitrin-3-O- β-sophoroside - Leaves Salem et al.95 Ribitol (%) 1.1 Leaves Salem et al.94 Ribofuranose (%) 0.8 Leaves Salem et al.94 Ribono-1, 4-lactone (%) 0.5 Leaves Salem et al.94 Soluble tannins (g/kg dry matter) 110.0 Leaves Dereje and Udén19 Sorbose (%) 0.4 Leaves Salem et al.94 Stachydrine - Bark and leaves Chini et al.62 Sucrose (%) 5.2 Leaves Salem et al.94 Talopyranose (%) 1.4 Leaves Salem et al.94 Tamarixetin-7-O-methylether - Leaves Salem et al.95 Tamarixetin-3-O-β-sophoroside-7-O-methylether - Leaves Salem et al.95 Tetrahydroxy-2-furanacetaldehyde (%) 0.8 Leaves Salem et al.94 Threonic acid (%) 0.6 Leaves Salem et al.94 Total extractable phenolics (mg/g dry matter) 13.1 Leaves Osuga et al.20 Total extractable tannins (mg/g dry matter) 1.5 Leaves Osuga et al.20 Trehalose (%) 1.3 Leaves Salem et al.94 Turanose (%) 11.9 Leaves Salem et al.94 Water (g/100g) 81.5 Fruits Lemmens7 Xylose, methyloxime (%) 0.5 Leaves Salem et al.94

Biological activities of Boscia angustifolia Staphylococcus aureus, Pseudomonas aeruginosa, The following biological activities have been reported Escherichia coli and Streptococcus pneumoniae but did from the bark, inner bark, leaves, roots, stem bark, twig not show activity against Salmonella typhi at and whole plant part extracts and the compound 7,4'- concentrations ranging from 10 mg/ml to 120 mg/ml with dimethoxy quercetin isolated from B. angustifolia: minimum inhibitory concentration (MIC) values ranging antibacterial,55,59,66,67,96,97 antimycobacterial,67 antifungal,67 from 10.0 mg/ml to 20.0 mg/ml.59. Similarly, Hassan et antiviral,94 antioxidant,94 antiplasmodial,74,79,98,99 al.96 evaluated antibacterial activities of chloroform root 75,100 antitrypanosomal, GABAA–benzodiazepine receptor extracts of B. angustifolia against Staphylococcus aureus, binding,98 larvicidal100 and cytotoxicity94,99,102 activities. Pseudomonas aeruginosa, Escherichia coli, Salmonella typhi and Streptococcus pneumoniae using the micro Antibacterial activities dilution technique with tetracycline (10 mg/mL) as a Elegami et al.55 evaluated antibacterial activities of positive control. The extract exhibited activities against aqueous, chloroform and methanol whole plant part Staphylococcus aureus, Pseudomonas aeruginosa, extracts of B. angustifolia against Bacillus subtilis, Escherichia coli and Streptococcus pneumoniae but did Staphylococcus aureus, Escherichia coli and not show activity against Salmonella typhi at Pseudomonas aeruginosa using cup-plate agar diffusion concentrations of 5 mg/mL to 60 mg/mL with MIC values method with ampicillin and neomycin as positive controls. ranging from 0.6 mg/mL to 1.3 mg/mL.96 Maregesi et al.97 The chloroform and methanol extracts exhibited activities evaluated antibacterial activities of aqueous, n-hexane and with zone of inhibition ranging from 13 mm to 18 mm methanol stem bark extracts of B. angustifolia against which was comparable to 11 mm to 23 mm exhibited by Bacillus cereus, Staphylococcus aureus, Escherichia coli, the positive controls.55 Hassan et al.59 evaluated Pseudomonas aeruginosa, Klebsiella pneumoniae and antibacterial activities of aqueous, hexane, petroleum ether Salmonella typhimurium using a liquid dilution method and chloroform root extracts of B. angustifolia against with ampicillin and rifampicin as positive controls. The n- Staphylococcus aureus, Pseudomonas aeruginosa, hexane extract exhibited activities against Bacillus cereus Escherichia coli, Salmonella typhi and Streptococcus with MIC and minimum bactericidal concentration (MBC) pneumoniae using the micro dilution technique with value of 500 µg/mL while MIC value of 1000 µg/mL was tetracycline (10 mg/ml) as a positive control. The aqueous exhibited against Staphylococcus aureus.97 Omwenga et and chloroform extracts were active against al.66 evaluated antibacterial activities of methanol bark

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extracts of B. angustifolia against Staphylococcus aureus, maximal inhibitory concentration (IC50) values of 41.2 Bacillus subtillis, Salmonella typhi, Escherichia coli and μg/ml and 16.5 μg/ml, respectively which were higher that Pseudomonas aeruginosa using disc diffusion and micro IC50 value of 1.9 μg/ml exhibited by the positive control, titre-dilution techniques with amoxicillin and cefrodoxima ascorbic acid.94 as positive controls. The extracts exhibited activities against tested pathogens with zone of inhibition ranging Antiplasmodial activities from 7.0 mm to 20.0 mm which was comparable to 17.1 Koch et al.74 evaluated antiplasmodial activities of mm to 24.2 mm exhibited by amoxicillin. The MIC value chloroform inner bark extracts of B. angustifolia against a against the tested pathogens was 3.8 mg/50μl while the chloroquine-sensitive (D6) strain of Plasmodium MBC values ranged from 3.8 mg/50μl to 7.5 mg/50μl.66. falciparum using a semiautomated microdilution 67 Mariita et al. evaluated antibacterial activities of technique. The extract showed activity with an IC50 value methanolic bark extracts of B. angustifolia against of >10.0 μg/ml.74 Bah et al.98 evaluated the antiplasmodial Salmonella typhi, Staphylococcus aureus, Pseudomonas activities of dichloromethane and methanol bark and leaf aeruginosa, Escherichia coli and Klebsiella pneumoniae extracts of B. angustifolia against the chloroquine using the agar disc diffusion method with amoxicillin and sensitive strain of Plasmodium falciparum (3D7) using the ciprofloxacin as positive controls. The extract exhibited parasite lactate dehydrogenase (pLDH) assay. The activities against tested pathogens with zone of inhibition methanol leaf extract exhibited moderate activities with 98 79 ranging from 6.7 mm to 9.0 mm which was lower than IC50 value of 37.6 μg/ml. Muthaura et al. and Muthaura 13.0 mm to 21.3 mm exhibited by the positive controls. et al.99 evaluated antiplasmodial activities of aqueous and The MIC and MBC values exhibited against methanol stem bark extracts of B. angustifolia against Staphylococcus aureus were 37.5 mg/mL and 75.0 chloroquine sensitive (D6) and resistant (W2) Plasmodium mg/mL, respectively.67 falciparum using the semi-automated micro-dilution technique that measures the ability of the extracts to Antimycobacterial activities inhibit the incorporation of (G-3H) hypoxanthine into the Mariita et al.67 evaluated antimycobacterial activities of malaria parasite. The aqueous and methanol extracts methanolic bark extracts of B. angustifolia against exhibited activities with IC50 values of 1.4 μg/ml and 7.4 Mycobacterium tuberculosis, Mycobacterium Kansasii, μg/ml, respectively against D6, and 4.7 μg/ml and 35.9 Mycobacterium fortuitum and Mycobacterium smegmatis μg/ml, respectively against W2.79,99 Muthaura et al.99 using the BACTEC MGIT 960 system with isoniazid as a evaluated the in vivo antimalarial activities of aqueous and positive control. At the highest concentration of 2.0 methanol stem bark extracts of B. angustifolia by using mg/mL, the extract exhibited activities against tested chloroquine sensitive Plasmodium berghei strain ANKA pathogens.67 based on four-day suppressive test. The methanol extract was active in interperitonial injection treatment with Antifungal activities chemo-suppression of 60.1% which was lower than 99.9% Mariita et al.67 evaluated antifungal activities of chemo-suppression of malaria parasites exhibited by the methanolic bark extracts of B. angustifolia against positive control, chloroquine.99 Candida albicans, using the agar disc diffusion method with fluconazole as a positive control. The extract Antitrypanosomal activities exhibited activities against the tested pathogen with zone Bizimana et al.75 evaluated the antitrypanosomal activities of inhibition of 6.0 mm which was lower than 13.0 mm of water, methanol and dichloromethane leaf and twig exhibited by the positive control.67 extracts of B. angustifolia using the low inoculation long Incubation test (LILIT) with diminazene aceturate as a Antiviral activities positive control. All the extracts exhibited activities with Salem et al.94 evaluated the antiviral activities of aqueous MIC value of 10.0 μg/ml while diminazene aceturate methanol leaf extracts of B. angustifolia and the exhibited MIC value of 0.05 μg/ml.75 Aderbauer et al.100 compound 7,4'-dimethoxy quercetin isolated from the evaluated antitrypanosomal activities of dichloromethane species against avian influenza virus (H5N1) using plaque stem bark extracts of B. angustifolia using the long-term reduction assay. Both the extract and the compound 7,4'- viability assay on Trypanosoma brucei brucei. The dimethoxy quercetin exhibited activities with a potential extracts exhibited activities with minimum toxic activity against H5N1 infection up to 63 and 68.5%, concentration (MTC) and MIC values of 100.0 μg/ml and respectively, at concentration of 80 μg/μl.94 200.0 μg/ml, respectively.100

Antioxidant activities GABAA–benzodiazepine receptor binding activities 94 98 Salem et al. evaluated the antioxidant activities of Bah et al. evaluated the GABAA–benzodiazepine aqueous methanol leaf extracts of B. angustifolia and the receptor binding activities of dichloromethane and compound 7,4'-dimethoxy quercetin isolated from the methanol bark and leaf extracts of B. angustifolia using species using 2,2-diphenyl-1-picrylhydrazyl (DPPH) the GABAA–benzodiazepine receptor binding assay. A radical scavenging assay with ascorbic acid as a positive weak GABAA-receptor complex binding activity was control. Both the extract and the compound 7,4'- exhibited by dichloromethane leaf extract.98 dimethoxy quercetin exhibited activities with half

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Larvicidal activities REFERENCES Cepleanu et al.101 evaluated larvicidal activities of [1] Hall, J.C., Sytsma, K.J., Iltis, H.H., Amer. J. Bot. 2002, 89, 1826- aqueous, dichloromethane and methanol root bark and 1842. [2] Kers, L.E., in: Kubitzki, K., Bayer, C. (Eds.), The Families and stem bark extracts of B. angustifolia by assessing the Genera of Vascular , Vol. 5, Springer-Verlag, Berlin 2003, effect of extracts at a concentration of 500 mg/ml on pp. 36-56. mortality of 2nd instar larvae of Aedes aegypti with [3] Hall, J.C., Bot. 2008, 86, 682-696. diazinon as a positive control. Only dichloromethane root [4] Schmidt E, Lötter M, McCleland W. Trees and Shrubs of Mpumalanga and Kruger National Park, Jacana Media, bark extract exhibited weak activities with LC100 value Johannesburg 2002. after 24 hours of 250.0 μg/ml which was higher than LC100 [5] Kamel, W.M., El-Ghani, M.M.A., El-Bous, M.M., Afr. J. Pl. Sci. value of 0.1 μg/ml exhibited by the positive control.101 Biotechnol. 2009, 3, 27-35. u[6] Iw , M.M., Handbook of African Medicinal Plants, CRC Press, Boca Raton 2014. Cytotoxicity activities [7] Lemmens, R.H.M.J., in: Schmelzer, G.H., Gurib-Fakim, A. (eds.), 102 Hassan et al. evaluated the toxicological effects of the Plant Resources of Tropical Africa 11: Medicinal Plants 2, alkaloid and aqueous ethanol root extracts of B. Backhuys Publishers, Leiden 2013, pp. 21-22. angustifolia on biochemical indices of kidney and liver [8] Lemmens, R.H.M.J., in: Schmelzer, G.H., Gurib-Fakim, A. (eds.), Plant Resources of Tropical Africa 11: Medicinal Plants 2, functions in Wister albino rats. The renal and liver indices Backhuys Publishers, Leiden 2013, pp. 22-25. were significantly altered at higher doses of alkaloidal [9] Storrs, A.E.G., Know your Trees: Some of the Common Trees extract at 703.6 mg/kg and 1125.7 mg/kg, and aqueous Found in Zambia, Forest Department, Ndola 1979. methanol extract at 839.3 mg/kg and 1342.8 mg/kg body [10] Burkill, H.M., The Useful Plants of West Tropical Africa, Volume 1, Families A–D, Royal Botanic Gardens, Kew, London 1985. weight. The extracts produced histopathological lesions of [11] Kalikawa, M.C., Afr. J. Ecol. 1990, 28, 253‐256. the liver and kidney such as perivascular cuffs, protein [12] Skarpe, C., J. Appl. Ecol. 1990, 27, 873‐885. cast, infiltration, slight infiltration at higher doses. There [13] Nott, T.B., Stander, P.E., Madoqua 1991, 18, 11‐15. was a significant dose dependent decrease in weight in the [14] Bein, E., Habte, B., Jaber, A., Birnie, A., Tengnas, B., Useful 102 99 Trees and Shrubs in Eritrea: Identification, Propagation and rats given higher doses of the extract. Muthaura et al. Management for Agricultural and Pastoral Communities, evaluated the cytotoxicity activities of aqueous and Regional Soil Conservation Unit, Technical Handbook Series 12, methanol stem bark extracts of B. angustifolia on Vero Nairobi 1996. cells using the plaque reduction assay. The methanol and [15] Brundin, J., Karlsson, P., Browse and Browsers in South-Western Kalahari: Minor Field Studies, Swedish University of water extracts were non-toxic with CC50 value of 1000.0 99 94 Agricultural Sciences, Report no. 73, Uppsala 1999. µg/mL and 6720.0 µg/mL, respectively. Salem et al. [16] Pakia, M., Cooke, J.A., S. Afr. J. Bot. 2003, 69, 370–381. evaluated cytotoxicity activities of aqueous methanol leaf [17] Arbonnier, M., Trees, Shrubs and Lianas of West African Dry extracts of B. angustifolia and the compound 7,4'- Zones, CIRAD, Paris 2004. [18] Lykke, A.M., Kristensen, M.K., Ganaba, S., Biod. Cons. 2004, 13, dimethoxy quercetin isolated from the species using the 3- 1961–1990. (4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium [19] Dereje, M., Udén, P., Animal Feed Sci. Technol. 2005, 121, 297– bromide (MTT) assay. Both the extract and the compound 308. [20] Osuga, I.M., Abdulrazak, S.A., Nishino, N., Ichinohe, T., 7,4'-dimethoxy quercetin exhibited activities with TC50 94 Fujihara, T., Livestock Res. Rural Develop. 2006, 18, 12. values of 151.0 μg/μl and 81.0 μg/μl, respectively. [21] Ogbazghi, W., Bein, E., in: Ghebru, B., Mehari, T. (Eds.), Innovative Agricultural Approaches of Promoting Food Security CONCLUSION in Eritrea: Trends, Challenges and Opportunities for Growth, The present review summarizes the botany, medicinal Geographica Bernensia, Bern 2007, pp. 29-40. [22] Theilade, I., Hansen, H.H., Krog, M., Ruffo, C.K., For. Trees uses, phytochemistry and pharmacological properties B. Livel. 2007, 17, 109-123. angustifolia. Based on presented information, there is not [23] Zorloni, A., Evaluation of Plants Used for the Control of Animal yet enough data correlating the ethnomedicinal uses of the Ectoparasitoses in Southern Ethiopia (Oromiya and Somali species with its phytochemical and pharmacological Regions), MSc Dissertation, University of Pretoria, Pretoria 2007. [24] Orwa, C., Mutua, A., Kindt, R., Jamnadass, R., Anthony, S., properties. Detailed studies on the pharmacokinetics, in Boscia angustifolia A. Rich. (Capparidaceae): Agroforestry vivo and clinical research involving both extracts and Database: A Tree Reference and Selection Guide Version 4.0, compounds isolated from the species are required. 2009, available at: Therefore, future research should focus on the molecular http://www.worldagroforestry.org/sites/treedbs/treedatabases.asp, accessed on 14 August 2019. modes or mechanisms of action, pharmacokinetics and [25] Assefa, A., Abebe, T., J. Sci. Develop. 2010, 1, 5-19. physiological pathways for specific extracts of the species [26] Sop, T.K., Oldeland, J., Bognounou, F., Schmiedel, U., including identification of the bioactive compounds of the Thiombiano, A., Environ. Dev. Sustain. 2012, 14, 627-649. species and their associated pharmacological activities. [27] Gidey, M., Beyene, T., Signorini, M.A., Bruschi, P., Yirga, G., J. Med. Plants Res. 2015, 9, 494-509. [28] National Research Council, Lost Crops of Africa: Vol 3: Fruits, Conflict of interest National Academy Press, Washington DC 2008. The author declares that there is no conflict of interest [29] Morgan, W.T.W., Econ. Bot. 1981, 35, 96-130. regarding the publication of this paper. [30] Apoorva, H.A., Mehdi, S., Krishna, K.L., Nabeel, K., Asian J. Pharm. Clinical Res. 2019, 12, 8-14. [31] Maity, D., Sandur, V.R., Asian J. Pharm. Clinical Res. 2019, 12, Figure legend 19-26. Figure 1. Medicinal applications of Boscia angustifolia [32] Quattrocchi, U., CRC World Dictionary of Medicinal and derived from literature records Poisonous Plants: Common Names, Scientific Names, Eponyms, Synonyms and Etymology, Taylor and Francis Group, Boca Raton 2012.

3426 Alfred Maroyi /J. Pharm. Sci. & Res. Vol. 11(10), 2019, 3420-3428

[33] Hyde, M.A., Wursten, B.T., Ballings, P., Palgrave, C.M., Boscia [63] Diallo, D., Hveem, B., Mahmoud, M.A., Berge, G., Paulsen, B.S., angustifolia A. Rich. var. corymbosa (Gilg) DeWolf: Flora of Maiga, A., Pharm. Biol. 1999, 37, 80-91. Zimbabwe, 2019, available at: [64] Ahua, K.M., Ioset, J.-R., Ioset, K.N., Diallo, D., Mauël, J., https://www.zimbabweflora.co.zw/speciesdata/species.php?specie Hostettmann, K., J. Ethnopharmacol. 2007, 110, 99–104. s_id=124490, accessed on 18 August 2019. [56] Maregesi, S.M., Ngassapa, O.D., Pieters, L., Vlietinck, A.J., J. [34] Wild, H., in: Exell, A.W., Wild, H. (Eds.), Flora Zambesiaca: Ethnopharmacol. 2007, 113, 457–470. Vol 1, Part 1, Flora Zambesiaca Managing Committee, London [66] Omwenga, E.O., Okemo, P.O., Mbugua, P.K., Ogol, C.K.P., 1960, pp. 194–245. Pharmacog. Mag. 2009, 4, 165-176. [35] Elffers, J., Graham, R.A., De Wolf, G.P., in: Hubbard, C.E., [67] Mariita, R.M., Ogol, C.K.P.O., Oguge, N.O., Okemo, P.O., Res. J. Milne-Redhead, E. (Eds.), Flora of Tropical East Africa, Crown Med. Pl. 2011, 5, 54-64. Agents for Oversea Governments and Administrations, London [68] Omwenga, E.O., Mbugua, P.K., Okemo, P.O., Res. Rev. J. Bot. 1964, pp.1-88. Sci. 2014, 3, 25-29. [36] Palmer, E., Pitman, P., Trees of Southern Africa Covering all [69] Gebrezgabiher, G., Kalayou, S., Sahle, S., Int. J. Biod. Cons. Known Indigenous Species in the Republic of South Africa, South 2013, 5, 89-97. , Botswana, Lesotho and Swaziland, AA Balkema, [70] Fowler, D.G., Traditional Fever Remedies: A List of Zambian Cape Town 1972. Plants, Royal Botanical Gardens, Kew, London 2006. [37] Fici, S., Thulin, M., Kers, L.E., in: Thulin, M. (Ed.), Flora of [71] Chinsembu, K.C., Syakalima, M., Semenya, S.S., S. Afr. J. Bot. Somalia: Vol 1: Pteridophyta, Gymnospermae, Angiospermae 2019, 122, 369-384. (Annonaceae-Fabaceae), Royal Botanic Gardens, Kew, London [72] Ajayi, T.O., Moody, J.O., Anthony, C.S., Nig. J. Pharm. Res. 1993, pp. 37–60. 2019, 15, 61-73. [38] Palgrave, M.C., Keith Coates Palgrave Trees of Southern Africa, [73] Mathias, M.E., Taxon 1982, 31, 488-494. Struik Publishers, Cape Town 2002. 4[7] Koch, A., Tamez, P., Pezzuto, J., Soejarto, D., J. Ethnopharmacol. [39] Germishuizen, G., Meyer, N.L., Plants of Southern Africa: An 2005, 101, 95-99. Annotated Checklist, Strelitzia 14, National Botanical Institute, [75] Bizimana, N., Tietjen, U., Zessin, K.-H., Diallo, D., Djibril, C., Pretoria 2003. Melzig, M.F., Clausen, P.H., J. Ethnopharmacol. 2006, 103, 350– [40] Darbyshire, I., Kordofani, M., Farag, I., Candiga, R., Pickering, 356. H., The Plants of Sudan and South Sudan, Kew Publishing, Kew, [76] Kokwaro, J.O., The Medicinal Plants of East Africa, University of London 2015. Nairobi Press, Nairobi 2009. [41] Van Wyk, B., Van Wyk, P., Field Guide to Trees of Southern [77] Chinsembu, K.C., Acta Tropica 2015, 152, 32–48. Africa, Struik Publications (Pty) Ltd, Cape Town 1997. [78] Diarra, N., Van’t Klooster, C., Togola, A., Diallo, D., Willcox, [42] Drummond, R.B., Kirkia 1975, 10, 229-285. M., de Jong, J., J. Ethnopharmacol. 2015, 166, 352–360. [43] Mapaura, A., Timberlake, J., A Checklist of Zimbabwean Vascular [79] Muthaura, C.N., Keriko, J.M., Mutai, C., Yenesew, A., Gathirwa, Plants, Southern African Botanical Diversity Network Report No. J.W., Irungu, B.N., Nyangacha, R., Mungai, G.M., Derese, S., J. 33, Pretoria 2004. Ethnopharmacol. 2015, 175, 315–323. [44] Setshogo, M.P., Preliminary Checklist of the plants of Botswana, [80] Danton, O., Somboro, A., Fofana, B., Diallo, D., Sidibé, L., Southern African Botanical Diversity Network Report No. 37, Rubat-Coudert, C., Marchand, F., Eschalier, A., Ducki, S., Pretoria 2005. Chalard, P., J. Herbal Med. 2019, [45] Mannheimer, C.A., Curtis, B.A., Le Roux and Müller's Field https://doi.org/10.1016/j.hermed.2019.100271. Guide to the Trees and Shrubs of Namibia, Macmillan Education [81] Menge, D.M.S., Makobe, M., Monda, E.O., Okemo, P.O., Afr. J. Namibia, Windhoek 2009. Pl. Sci. 2014, 8, 356–363. [46] Burrows, J.E., Burrows, S.M., Lötter, M.C., Schmidt, E., Trees [82] Karani, A.O., Ndakidemi, P.A., Mbega, E.R., J. Appl. Life Sci. Int. and Shrubs of Mozambique, Publishing Print Matters (Pty), Cape 2017, 12, 1-10. Town 2018. 3[8] Otieno, J.N., Magadula, J.J., Kakudidi, E., Kirimhuzya, C., [47] Gelfand, M., Drummond, R.B., Mavi, S., Ndemera, B., The Orodho, J., Okemo, P., Int. J. Biod. Cons. 2011, 3, 610-617. Traditional Medical Practitioner in Zimbabwe: His Principles of [84] Legesse, G.A., Plant Diversity and Ethnobotany of Medicinal and Practice and Pharmacopoeia, Mambo Press, Gweru 1985. Wild Edible Plants in Amaro District of Southern Nations, [48] Zenebe, G., Zerihun, M., Solomon, Z., Ethnobot. Res. Appl. 2012, Nationalities and Peoples Region and Gelana District of Oromia 10, 305-320. Region, Southern Ethiopia, PhD Thesis, Addis Ababa University, [49] Enyew, A., Asfaw, Z., Kelbessa, E., Nagappan, R., Curr. Res. J. Addis Ababa 2017. Biol. Sci. 2014, 6, 154-167. [85] Kaingu, C.K., Oduma, J.A., Kanui, T.I., J. Ethnopharmacol. 2011, [50] Chekole, G., Asfaw, Z., Kelbessa, E., J. Ethnobiol. Ethnomed. 137, 495-502. 2015, 11, 4. [86] Kaushik, A., Ambesajir, A., Kaushik, J.J., Girmay, B., Asian J. [51] Gidey, M.H., Asfaw, Z., Adv. J. Biol. Sci. Res. 2015, 3, 8-36. Biomed. Pharmaceut. Sci. 2013, 3, 1-6. [52] Hishe, M., Asfaw, Z., Adv. J. Biol. Sci. Res. 2015, 3, 37-40. [87] Doka, I.G., Yagi, S.M., Ethnobot. Leaflets 2009, 13, 1409-1416. [53] Mekuanent, T., Zebene, A., Solomon, Z., J. Nat. Remedies 2015, [88] Tefera, B.N., Kim, Y.-D., J. Ethnobiol. Ethnomed. 2019, 15, 25. 15, 88-112. [89] Chinsembu, K.C., Hedimbi, M., Mukaru, W.C., J. Med. Pl. Res. [54] Fitsumbirhan, T., Mebrahtom, M., Semere, T., Int. J. Ophthalmol. 2011, 5, 6787-6797. Visual Sci. 2017, 2, 80-87. [90] Tsigemelak, D., Dharani, N., Kinyamario, J.I., Kiboi, S., Int. J. Pl. [55] Elegami, A.A., Almagboul, A.Z., Omer, M.E.A., El Tohami, Animal Environ. Sci. 2016, 5, 151-159. M.S., Fitoterapia 2001, 72, 810-817. [91] Pare, D., Hilou, A., Ouedraogo, N., Guenne, S., Medicines 2016, [65] Keay, R.W., Onochie, C.F., Stanfield, D.P., Nigerian Trees, 3, 9. Ibadan: Federal Department of Forest Research, Lagos 1960. 2[9] Byaruhanga, C., Ndukui, J.N., Olinga, S., Egayu, G., Boma, P., [57] Diallo, D., Sogn, C., Samaké, F.B., Paulsen, B.S., Michaelsen, Aleper, D., Livestock Res. Rural Develop. 2015, 27, 8. T.E., Keita, A., Pharm. Biol. 2002, 40, 117-128. [93] Kigen, G., Kamuren, Z., Njiru, E., Wanjohi, B., Kipkore, W., [58] Fowler, D.G., Kirkia 2002, 18, 35-48. Evidence-Based Compl. Alt. Med. 2019, vol 2019, art. ID [59] Hassan, S.W., Umar, R.A., Lawal, M., Bilbis, L.S., Muhammad, 8976937. B.Y., Dabai, Y.U., Afr. J. Biotechnol. 2006, 5, 1602–1607. [94] Salem, M.M., Hussein, S.R., El-Sharawy, R., El-Khateeb, A., [60] Cheruiyot, K.J., Elizabeth, N., Charles, M., Christine, B., Richard, Ragab, E.A., Dawood, K.M., El Negoumy, S.I.M., Egyptian K., Emily, T., J. Ethnobiol. Trad. Med. Photon 2013, 120, 633- Pharmaceut. J. 2016, 15, 1–5. 649. [95] Salem, M.M., Hussein, S.R., El-Sharawy, R., Ragab, E.A., [61] Chalo, M.D., Camilla, B., Mutiso, C.P., Int. J. Pharmacol. Res. Dawood, K.M., El Negoumy, S.I.M., Biochem. Syst. Ecol. 2016, 2016, 6, 68-74. 65, 202-204. [62] Chini, C., Bilia, A.R., Keita, A., Morelli, I., Planta Med. 1992, 58, [96] Hassan, S.W., Lawal, M., Muhammad, B.Y., Umar, R.A., Bilbis, 476. L.S., Ebbo, A.A., Dabai, Y.U., J Pharm. Toxicol. 2007, 2, 366– 372.

3427 Alfred Maroyi /J. Pharm. Sci. & Res. Vol. 11(10), 2019, 3420-3428

[97] Maregesi, S.M., Pieters, L., Ngassapa, O.D., Apers, S., [100] Aderbauer, B., Clausen, P.-H., Kershaw, O., Melzig, M.F., J. Vingerhoets, R., Cos, P., Van den Berghe, D.A., Vlietinck, A.J., J. Ethnopharmacol. 2008, 119, 225-231. Ethnopharmacol. 2008, 119, 58–66. [101] Cepleanu, F., Hamburger, M.O., Sordat, B., Msonthi, J.D., Gupta, [98] Bah, S., Jäger, A.K., Adsersen, A., Diallo, D., Paulsen, B.S., J. M.P., Saadou, M., Hostettmann, K., Int. J. Pharmacog. 1994, 32, Ethnopharmacol. 2007, 110, 451–457. 294-307. [99] Muthaura, C.N., Rukunga, G.M., Chhabra, S.C., Omar, S.A., [102] Hassan, S.W., Umar, R.A., Lawal, M., Bilbis, L.S., Muhammad, Guantai, A.N., Gathirwa, J.W., Tolo, F.M., Mwitari, P.G., Keter, B.Y., Faruk, U.Z., Ebbo, A.A., Asian J. Biochem. 2006, 1, 287- L.K., Kirira, P.G., Kimani, C.W., Mungai, G.M., Njagi, E.N., 296. Phytother. Res. 2007, 21, 860–867.

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